Microbiologic Analysis of Hand Infections: A Prospective Study

Abstract

Background:

Hand infections are a common problem in emergency departments. Staphylococcus aureus is the main pathogen of both hand and blood stream infections. Therefore, the aim of the present study was to evaluate the frequency and impact of bacteremia in patients with hand infections to improve the microbiologic diagnostics.

Patients and Methods:

A prospective study of 90 patients with acute hand infections without antimicrobial pre-treatment was performed. Blood cultures were taken pre-operatively. If positive, transesophageal echocardiography was performed to rule out infectious endocarditis. Tissue samples were microbiologically processed using standardized culture media. If negative, a broad-spectrum bacterial 16S ribosomal RNA (rRNA) gene polymerase chain reaction (PCR) was applied. The etiology and location of the infection, the length of hospital stay, the number of surgical interventions, and the inflammatory parameters were obtained.

Results:

Six patients with bacteremia (6.6%) were diagnosed, after animal bites (n = 3) and intra-articular empyema (n = 3). Pathogens included Staphylococcus pettenkoferi, Pasteurella multocida, Staphylococcus epidermidis, Staphylococcus aureus, and Bacteroides pyogenes. No case of infective endocarditis was detected. Patients with bacteremia required more surgical interventions (p = 0.002), had a longer hospital stay (p < 0.001), higher plasma C-reactive protein (CRP; p = 0.016), and a higher age (p = 0.002) compared with those without bacteremia. In 14 cases (15.6%) no pathogen was detected by culture, whereas the subsequent broad-spectrum PCR diagnosed three cases (21.4%).

Conclusions:

Pre-operative blood cultures in patients with hand infections are important to detect bacteremia as an essential marker of clinical severity. Those blood cultures are indicated after deep animal bites and joint empyema. A precise identification of pathogens is fundamental for an effective treatment of hand infections, for which a 16S rRNA gene PCR can contribute in culture-negative tissue samples.

Up to 25% of patients presenting in hand surgery departments suffer from hand and upper extremity infections.¹ An inadequate or delayed treatment may lead to impaired hand function due to stiff joints, contractures, or ultimately, amputations.² Therefore, a thorough understanding of the spread of the infection and a precise determination of pathogens are of utmost importance. Currently, microbiologic cultures from intra-operative swabs and tissue specimen are standard for microbiologic diagnostics. However, in 20% to 70% of patients with hand infections no pathogen is detected using these methods.^3–7 Pasteurella multocida is the most common isolated pathogen in hand infections due to animal bites,⁸ whereas Staphylococcus aureus is encountered most frequently in hand infections from other etiologies.⁶ The latter is, moreover, the most important pathogen in blood stream infections and infective endocarditis.⁹ Blood stream infections represent one of the leading causes of death in Europe with an estimated 1,200,000 cases, of which 13% are lethal.¹⁰ The most common foci are skin and soft tissue infections as well as catheter-associated infections.⁹ Furthermore, blood stream infections are the leading cause of infective endocarditis,¹¹ the major sequelae of which is valve insufficiency.¹²

Because a high percentage of negative results using culture methods may occur in hand infections, we evaluated the value of an additional broad-spectrum bacterial 16S ribosomal RNA (rRNA) gene polymerase chain reaction (PCR) in culture negative tissue samples. In addition, the frequency and impact of bacteremia in hand infections were analyzed to estimate the rate of systemic manifestations associated with hand infections.

Patients and Methods

Participants

A prospective cohort of 90 patients with hand infections was evaluated at a single institution from February 2019 to August 2021. This study was approved by the local ethics committee review board (approval number EK-BR-106/18-2). Informed consent was obtained from all participants who took part in this study. Exclusion criteria were any antimicrobial pre-treatment, pre-diagnosed infective endocarditis, pregnancy, and age <18 years. Patients were assigned to one of the following three groups: hand infection after animal bite, palmar, and dorsal hand infection from other etiologies. This differentiation was based on the fact that animal bites have a different microbial spectrum and palmar side infections spread rapidly because of the close location of the synovial flexor tendon sheaths in the carpal tunnel. The infection mechanism and the time elapsed between the onset of infection and presentation in the emergency department were documented. Because the study was performed during time periods both before and after the coronavirus disease 2019 (COVID-19) pandemic, the duration between trauma and presentation at the hospital for both time periods was also analyzed comparatively. Pre-operatively, blood was drawn for the blood cultures and for the determination of laboratory inflammatory parameters.

Surgical intervention

All hand infections underwent surgical intervention. The wounds were radically debrided, excising the complete necrotic and infected tissue. Representative infected tissue samples were taken from the depth of the wound for microbiologic analysis. The wounds were irrigated. Finally, the wounds were sutured.

Post-operatively, the hands were immobilized until the local infection subsided. Parts of the tissue samples were stored at −20°C to perform a broad-spectrum 16S rRNA gene PCR in cases in which the culture results were negative. Systemic intravenous antimicrobial agents were initiated immediately after intra-operative sampling. Considering potential pathogen spectrum and local antimicrobial resistance, epidemiology ampicillin-sulbactam was used as an empiric antimicrobial therapy. If a penicillin allergy was present, clindamycin was prescribed. Criteria for a second look after 48 hours were severe infections with ongoing purulent discharge. The number of surgical interventions and the length of the hospital stay were evaluated.

Microbiology and transesophageal echocardiography

Two aerobic and anaerobic blood cultures were drawn for the detection of bacteremia. For patients with bacteremia transesophageal echocardiography (TEE) was performed to diagnose infectious endocarditis. Debrided soft tissue samples and swabs taken intra-operatively were microbiologically cultured using standardized culture media. If negative, a broad-spectrum bacterial 16S rRNA gene PCR was performed. Antimicrobial treatment was adjusted according to susceptibility tests.

Data analysis

For descriptive statistics, the median with minimum and maximum was used. The Kolmogorov-Smirnov test was performed for analysis of the data distribution. The Kruskal-Wallis test followed by the Mann-Whitney test with post hoc Bonferroni adjustment were used. Nominal data were analyzed using the Fisher exact test. The level of significance was set at p ≤ 0.05.

Results

Anthropometric data

A total of 90 patients were included in the study. There were 30 patients with a hand infection after an animal bite, with a palmar or dorsal infection, respectively (Table 1). Animal bites were caused by cats in 21 cases, and dogs in eight cases. One human bite was documented. Table 2 summarizes the clinical data of all three groups as well as the injury mechanisms, of which one was a blunt trauma, four crush and 43 penetrating injuries. Minimal trauma was seen in two cases. No significant differences in patient presentations before and during the COVID-19 pandemic were found. The median interval from trauma to presentation was three days before and 3.5 days during the COVID-19 pandemic.

Table 1.

Anthropometric Data

Parameter	Hand infection
Parameter	Animal bite (n = 30), all locations	Other etiologies, palmar (n = 30)	Other etiologies, dorsal (n = 30)
Mean age (y)	51.3	58.1	54.4
Gender (n)
Male	17 (56.7%)	14 (46.7%)	23 (76.7%)
Female	13 (43.3%)	16 (53.3%)	7 (23.3%)
Nicotine abuse (n)	11 (36.7%)	8 (26.8%)	7 (23.3%)
Alcohol abuse (n)	3 (10%)	9 (30%)	7 (23.3%)

Table 2.

Clinical, Laboratory, and Basic Blood Culture Data of the Patients Included in the Study Cohort

Clinical parameter	Hand infection
Clinical parameter	Animal bite (n = 30)	Palmar (n = 30)	Dorsal (n = 30)
Primary injury (n)
Animal bite	30	0	0
Cut injury	0	12	12
Idiopathic	0	4	7
Foreign body	0	6	4
Post-operative	0	4	3
Insect bite	0	3	1
Infected calcinosis	0	1	1
Intravenous drug use	0	0	1
Infected burn	0	0	1
Soft tissue infection (n)	28	24	16
Bone involvement (n)	0	2	3
Intra-articular empyema (n)	2	4	11
Hospital length of stay (d)	5 (1–27)	7 (2–24)	7 (2–53)
Number of surgical interventions (n)	1 (1–4)	2 (1–5)	2 (1–6)
Interval from injury to surgical treatment (d)	1 (0–26)	6 (1–26)	5 (1–27)
CRP (mg/L)	7.7 (0.6–175.6)	14.1 (1–309.4)	16.5 (1.2–136.5)
Leukocyte count (Gpt/L)	10.3 (6.6–20.7)	9.3 (5.2–28.7)	9.8 (1.2–30.8)
Blood culture (n)
Negative	27	29	28
Staphylococcus aureus	0	0	2
Staphylococcus pettenkoferi	1	0	0
Staphylococcus epidermidis	0	1	0
Bacteroides pyogenes	1	0	0
Pasteurella multocida	1	0	0

CRP = C-reactive protein.

Bacteremia and infective endocarditis

Bacteremia was present in six individuals, after animal bites (n = 3) and with intra-articular empyema (n = 3). Pathogens comprised Staphylococcus pettenkoferi, Pasteurella multocida, Staphylococcus epidermidis, Staphylococcus aureus, and Bacteroides pyogenes (Table 2). In no case was infective endocarditis detected. Patients with bacteremia required more surgical interventions (median, 3.5 [range, 2–5] vs. median, 1 [range, 1–6]; p = 0.002; Fig. 1), had a longer hospital stay (median, 20 days [range, 8–31] vs. median, 6 days [range, 1–53]; p < 0.001; Fig. 2), a higher plasma C-reactive protein (CRP; median, 79.8 mg/L [range, 5.3–175.6] vs. 10.5 mg/L [range, 0.6–309.4]; p = 0.016; Fig. 3), and a higher age (median, 71 years [range, 53–84] vs. 54 years [19–88]; p = 0.002) compared with those without bacteremia. No significant differences were seen for the leucocyte and thrombocyte count, respectively. Furthermore, patients with bacteremia had a normal body temperature (median, 36.7°C [range, 36.2–37]) at admission to the hospital.

FIG. 1.

Number of surgical interventions. Patients with bacteremia required more surgical interventions compared with patients without (*p = 0.002). ○ = Outliers that are ≤1.5 times the interquartile range; □ = Outliers that are ≤3 times the interquartile range.

FIG. 2.

Length of hospital stay. Patients with bacteremia had a longer hospital stay compared with patients without (*p < 0.001). ○ = Outliers that are ≤1.5 times the interquartile range; □ = Outliers that are ≤3 times the interquartile range.

FIG. 3.

C-reactive protein (CRP) value. Bacteremic patients had higher CRP values compared with patients without bacteremia (*p = 0.016). ○ = Outliers that are less than or greater than 1.5 times the interquartile range; □ = Outliers that are less than or greater than 3 times the interquartile range.

Microbiological results

Overall, a total of 50 different pathogens were detected (Supplementary Table S1). Pasteurella multocida was responsible for hand infections after animal bites in 60% of cases (n = 18). In contrast, Staphylococcus aureus was found in 46.7% of hand infections (n = 28) from other etiologies. Methicillin-resistant Staphylococcus aureus (MRSA) was detected in one case. Twenty-nine cultures were polymicrobial (32.2%; two pathogens, n = 17; three pathogens, n = 8; less than three pathogens, n = 4; Supplementary Table S2). No pathogen was detected in 14 cases (15.6%). The following broad-spectrum bacterial 16S rRNA gene PCR diagnosed three positives of 14 samples, whereas Pasteurella multocida and Roseivirga spp. were detected once each in the group of animal bites and Legionella longbeachae was found in the group of palmar hand infections. Roseivirga spp. was detected in a hand infection after a dog bite.

No significant differences were seen between the patients with culture negative samples, monomicrobial, or polymicrobial samples in terms of length of hospital stay, number of surgeries, CRP, or leucocyte values. All patients with animal bites were treated with ampicillin-sulbactam, which was also the empiric antimicrobial therapy in 88.3% (n = 53) of hand infections of other etiologies. Clindamycin was used in 5% (n = 3) of cases because of penicillin allergy. Cefuroxime and cefazoline were used in 3.3% (n = 2) of cases, respectively. The precise reasons for the adjustment of the antimicrobial therapy and the associated pathogens are shown in Supplementary Table S3.

Discussion

Patients with bacteremia had a more severe course of infection in contrast to the patients without bacteremia. Thus, they needed more surgical interventions, had a longer hospital stay, and higher CRP values. Therefore, bacteremia is a negative prognostic factor and may indicate a systemic propagation of the infection. Bacteremia caused by Staphylococcus aureus was present in 6.7% of all cases, which accounts for one-third of all bacteremic cases. This is in line with previous studies identifying Staphylococcus aureus as the main cause of bacteremia.^9,11 No case of infective endocarditis was found, which implies a rapid control of bacteremia based on the effectiveness of the combined antimicrobial and surgical treatment. To the best of our knowledge, there are no studies about the incidence of bacteremia in patients with hand infections.

The Infectious Diseases Society of America recommends drawing blood cultures in patients with skin and soft tissue infections resulting from animal bites, immersion injuries and in patients with neutropenia, immunodeficiency, and malignancy on chemotherapy.^13,14 Applying those criteria to our patient cohort, half of the patients with a blood stream infection would not have been detected. Additional causes for bacteremia in this study were a foreign body and a cut injury.

It remains controversial whether blood cultures should be obtained in patients with skin and soft tissue infections or not. Arguments against blood culture analysis are the low positive rates, the consequent low-cost effectiveness, and the few implications for the further treatment because the antibiotic therapy usually covers the pathogens of the hand infection and the bacteremia.^15,16 In this study, antimicrobial treatment was only adjusted after the positive blood culture result was received. In this case Pasteurella multocida was detected, a switch from ampicillin-sulbactam to ciprofloxacin was necessary because of antimicrobial resistance. However, this study demonstrates that patients with bacteremia had a more severe course in terms of the number of surgical interventions and the length of hospital stay.

Pre-operative blood cultures in patients with hand infections can be obtained to assess the clinical course and to identify severe systemic infections as early as possible because of delayed increasing CRP and leucocyte count, which frequently do not correlate with the severity of the infection.⁶ Several models predict the risk of bacteremia. Using the Shapiro et al.¹⁷ model, only one of the six patients with bacteremia would have had an indication for blood cultures. Using the Bacteraemia Prediction Risk Model of the INFURG-SEMES group,^18,19 none of the patients would have had an indication for blood cultures. However, a main limitation of our study is that procalcitonin (PCT) was not determined, which also impacts the Risk Model of the INFURG-SEMES group. Procalcitonin is a sensitive parameter to predict the risk of bacteremia especially to differentiate between true bacteremias and contaminations.^17,20–22 Nevertheless, the diagnostic value of PCT has not yet evaluated for patients with hand infections in prospective randomized studies compared with other inflammatory parameters such as CRP.²³ Based on our results, blood cultures are recommended in patients after deep animal bites, according to the guidelines of the Infectious Diseases Society of America,¹³ and additionally in patients with intra-articular empyema.

The pathogen in the intra-operative samples was Staphylococcus aureus with 47.7% of non-animal bite cases and Pasteurella multocida in 60% of animal bite injuries. In 15.5% of the cases no pathogen was detected. Previous studies show comparable data: Staphylococcus aureus are detected in up to 60% in hand infections.^6,24,25 In our cohort, MRSA was not a significant pathogen because it was detected in only one case. In contrast to the United States, where the prevalence of community acquired MRSA is up to 70%, the prevalence of MRSA in Germany is lower by 6% to 8.5% and in most cases is hospital acquired.^25–27 Pasteurella multocida was isolated in 50% to 80% of cases in hand infections caused by animal bite injuries.^24,25 The frequency of sterile cultures in hand infections varies between 11% and 70%.^5–7

In contrast to the present analysis, those studies included patients who were already receiving antimicrobial agents. This might be the reason for the relatively low rate of culture-negative samples of 15.6% in our study. The frequency of sterile cultures depends strongly on the preoperative antimicrobial treatment. A recent study found 19% sterile cultures in patients with antimicrobial pre-treatment, but a frequency of 6% was observed without pre-operative antimicrobial treatment. Pre-treatment was associated with a significant odds ratio of 2.8 (95% confidence interval, 2.1–3.7) for sterile cultures. The frequency of resistant pathogens corresponded to the regional epidemiology. Regarding the occurrence of bacteremia, there was no difference between those groups, indicating that disease severity and host factors are main drivers for bacteremia.²⁸

Risk factors for culture negative samples include sampling errors, antimicrobial pre-treatment, as well as fastidious and slow growing pathogens.^29,30 Sterilely obtained tissue samples are preferred as specimen over swabs, because they are more likely to represent deep tissue infection, have a lower risk of contamination, and a higher sensitivity for fastidious pathogens.¹⁴ Therefore, we only used representative infected tissue samples from the wound depth of the wound for microbiologic analysis. A broad-spectrum bacterial 16S rRNA gene PCR was conducted for all culture-negative samples, detecting a pathogen in 21.4% of cases of culture-negative samples. A previous study investigated samples from patients with septic arthritis and found a rate of 9% PCR positive, but culture-negative samples.³¹ However, some patients were already receiving antimicrobial agents.

A broad-spectrum PCR in culture-negative samples is reported with a sensitivity rate of 42.9% and a specificity of 100%.³² Main advantages of the PCR analysis are the fast detection of pathogens and the determination of the pathogen load. Disadvantages of broad-spectrum PCR include the susceptibility to skin contamination, its costs, and the limited ability to test antimicrobial resistance.³¹ In addition, false-positive results may arise from the presence of bacterial DNA after cell death.³³ It is emphasized that a broad-spectrum PCR can be a useful tool in culture-negative samples in which a bacterial infection is highly expected.^32,33 Antimicrobial treatment decreases the morbidity in hand infections.³⁴ To optimize the initiated antibiotic therapy, pathogen identification is crucial. A broad-spectrum bacterial 16S rRNA gene PCR adds to the fast detection of pathogens in those settings.

The fact that different surgeons within the same department performed the surgeries is a considerable limitation to this study. Furthermore, the results of the microbiologic investigations depend on the quality and the site of the specimen collection. Moreover, patients with antimicrobial experience were excluded from this study, limiting the wide range of hand infections, because many patients with hand infections have already received their initial treatment in the emergency department or as outpatients. Further studies should investigate patients with hand infections in larger multicenter well-defined cohorts to evaluate the yield of blood cultures and to assess whether preoperative blood cultures are cost effective.

Footnotes

Acknowledgments

The authors thank Christian Retschke and Amani Al Meklef for logistic support.

Authors' Contributions

Data acquisition: Rein, Sorowka, Kremer. Data analysis and interpretation: Rein, Sorowka, Grünewald. Drafting and revising the manuscript: all authors. Final approval of the version to be submitted: all authors.

All authors made substantive intellectual contributions to this study, in conception and design. All authors have read and approved the final submitted manuscript.

Funding Information

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author Disclosure Statement

Susanne Rein, Anne Sorowka, Thomas Grünewald, and Thomas Kremer have no conflicts of interest, including no relevant financial interests, activities, relationships, and affiliations. The authors disclose any financial conflicts of interest that may influence interpretation of this study and/ or results.

Supplementary Material

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